Celiac Axis

The celiac axis supplies the stomach, liver, spleen, portions of the pancreas, and the proximal duodenum. It originates from the ventral portion of the abdominal aorta, near the level of T12 to L1, between the diaphragmatic crura. Its origin is encased in the median arcuate ligament, a dense, fibrous portion of the central posterior diaphragm draped across the aortic hiatus. In most patients, the celiac axis branches soon after its origin into the common hepatic, splenic, and left gastric arteries. In 1% of cases, the SMA arises from the celiac axis as well, forming a common celiomesenteric trunk.

The hepatic artery is usually the first branch of the celiac axis. It may also arise from the SMA (the so-called replaced right hepatic artery) in approximately 12% of cases. Additional variants include the replaced common hepatic artery (approximately 2.5%) and direct origin of the common hepatic artery from the aorta (approximately 2%). The common hepatic artery gives rise to the right gastric artery and the gastroduodenal artery, which further divides into the right gastroepiploic and superior pancreaticoduodenal arteries. The remaining proper hepatic artery gives rise to the cystic, right hepatic, and left hepatic arteries, which serve the gallbladder, the right and caudate hepatic lobes, and the middle and left hepatic lobes, respectively.

The second branch of the celiac axis is the splenic artery. Its first named branch is the dorsal pancreatic artery, supplying the posterior body and tail of the pancreas. Just before entering the splenic hilum, the splenic artery gives rise to the left gastroepiploic artery and multiple short gastric arteries, providing blood flow to the gastric fundus.

The final branch of the celiac axis is the left gastric artery. It courses cephalad and to the left to supply the gastric cardia and fundus along the lesser curvature of the stomach, joining centrally with the right gastric artery from the hepatic artery. In approximately 12% of the population, the left hepatic artery originates from the left gastric artery.

Superior Mesenteric Artery

The SMA arises from the aorta just distal to the celiac axis at the level of L1 to L2. It passes behind the neck of the pancreas, in front of the uncinate process, and over the third portion of the duodenum. Its first branch, the inferior pancreaticoduodenal artery, courses superiorly to join the superior pancreaticoduodenal artery (from the gastroduodenal) and forms the most proximal collateral pathway with the celiac axis. The central branches of the SMA supply the midgut from the ligament of Treitz to the midtransverse colon. These include the middle colic (serving the proximal two thirds of the transverse colon), right colic (mid-ascending and distal ascending colon), and ileocolic (distal ileum, cecum, appendix, and proximal ascending colon).

Inferior Mesenteric Artery

The IMA arises from the left side of the aorta 8 to 10 cm distal to the SMA at the level of L3. It travels caudad and to the left before dividing into the left colic and sigmoid arteries. The IMA supplies the distal third of the transverse colon, the descending and sigmoid colons, and the proximal rectum. It has anastomotic communications with the left branch of the middle colic from the SMA and with portions of the middle and inferior rectal arteries from the internal iliac.

Collateral Circulation

The mesenteric circulation has a redundant collateral network that serves to maintain perfusion even with compromise of the proximal main channels. The celiac axis and SMA communicate primarily via the superior and inferior pancreaticoduodenal arteries (via the gastroduodenal artery). The SMA and IMA communicate via the centrally located arch of Riolan (often referred to as the meandering mesenteric artery), as well as by the multiple communications at the periphery of the colon called the marginal arteries of Drummond. In addition to these collateral pathways, muscular branches of the aorta may contribute to intestinal perfusion, including the lumbar intercostal arteries, internal mammary arteries (via the deep epigastric arteries), middle sacral artery, and internal iliac arteries (via collaterals between the inferior and superior rectal arteries). Because of this plentiful collateral network, it is understandable that in most instances of gradual occlusion, at least two of the three major mesenteric orifices must be blocked to produce the clinical syndromes of chronic intestinal ischemia. In contrast, sudden occlusion of one widely patent vessel can cause acute ischemia because collaterals may be underdeveloped.

Pathophysiology

There are four primary causes of acute mesenteric ischemia (AMI): embolization to the SMA (approximately 50% of all cases), thrombosis of a preexisting atherosclerotic lesion at the origin of the vessel (20%), nonocclusive mesenteric ischemia (20%), and mesenteric venous thrombosis (10%).^5,6 In earlier series, the phenomenon of nonocclusive mesenteric ischemia was not well appreciated and was frequently misdiagnosed as acute venous occlusion. For example, Cokkinis⁷ reported in 1935 that acute mesenteric venous thrombosis accounted for the majority of cases of AMI.

Other unusual arteriopathies, such as Takayasus arteritis, fibromuscular dysplasia, and polyarteritis nodosa, may first present with intestinal ischemia. Isolated dissections of the SMA also have been reported,⁸ although the more common mechanism is extension of dissections of the descending thoracic aorta into the SMA and celiac axis.^9,10

If untreated, intestinal ischemia commonly leads to intestinal infarction. Tissue loss may result from both hypoxia during flow interruption and reperfusion injury once intestinal arterial blood flow is restored. Reperfusion injury is principally mediated by activation of the enzyme xanthine oxidase and the recruitment and activation of circulating polymorphonuclear neutrophils (PMNs).^11,12 In the presence of oxygen and hypoxanthine (a by-product of adenosine triphosphate metabolism), xanthine oxidase produces oxygen-derived free radicals that cause severe local tissue injury through lipid peroxidation, membrane disruption, and increased microvascular permeability.¹³ PMNs are attracted to reperfused tissue by the local secretion of cytokines (tumor necrosis factor-α, interleukin-1, platelet-derived growth factor) by ischemic endothelium.^14–16 Subsequent rolling, adherence, and activation of the PMNs in the microcirculation result in the secretion of myeloperoxidase, collagenases, and elastases that can further injure the already ischemic and vulnerable tissue.^17–19 Activation of the inflammatory cascade may also have systemic effects, with cardiac, pulmonary, and other organ system dysfunction.²⁰

Acute Mesenteric Arterial Embolism

Most mesenteric arterial emboli originate from left atrial or ventricular mural thrombi or cardiac valvular lesions. These thrombi are usually associated with cardiac dysrhythmias such as atrial fibrillation or hypokinetic regions from previous myocardial infarctions. The majority of mesenteric emboli lodge in the SMA because of its high basal flow and nearly parallel course to the abdominal aorta. Only 15% of SMA emboli remain impacted at the origin of the vessel. The majority of emboli progress distally 3 to 10 cm to the tapered segment of the SMA just past the origin of the middle colic artery (Figure 23-2). A substantial fraction (10% to 15%) of mesenteric emboli are associated with concurrent emboli to another arterial bed.²¹ Intestinal ischemia owing to embolic arterial occlusion can be compounded by reactive mesenteric vasoconstriction, which further reduces collateral flow and aggravates the ischemic insult.

FIGURE 23-2 Anteroposterior view of the aorta revealing embolic occlusion of the proximal superior mesenteric artery (SMA). Note the normal-appearing proximal jejunal arterial branches and then an abrupt cutoff of the SMA.

(From McKinsey JF, Gewertz BL: Acute mesenteric ischemia. Surg Clin North Am 77:307–318, 1997.)

Acute Mesenteric Arterial Thrombosis

Thrombosis of the SMA or the celiac axis is usually associated with preexisting arterial lesions. When carefully questioned, many of these patients have histories consistent with chronic mesenteric ischemia (CMI), including postprandial pain, weight loss, “food fear,” bloating, and early satiety. By far, the most common underlying lesion is an atherosclerotic plaque that slowly progresses to a critical stenosis over years, until the residual lumen suddenly thromboses during a period of low flow. Unlike embolic occlusions, thrombosis of the SMA generally occurs flush with the aortic origin of the vessel.

As noted previously, an unusual cause of AMI is aortic dissection involving the origins of the visceral vessels. The intimal flap of the dissection can exclude, compress, or extend into the visceral vessels, resulting in acute thrombosis. The symptoms of bowel ischemia may be masked by the pain associated with the aortic dissection, leading to a delay in diagnosis and treatment. AMI following coronary artery bypass grafts is rare but highly lethal, with mortality rates as high as 70%. As would be expected, ischemia occurs in patients with severely stenotic mesenteric vessels that occlude during the nonpulsatile perfusion of extracorporeal bypass.^22,23

Nonocclusive Mesenteric Ischemia

Mesenteric ischemia unassociated with anatomic arterial or venous obstruction can occur during periods of low cardiac output. Such low-flow states can result from cardiac failure, sepsis, or administration of α-adrenergic agents or digitalis compounds. Although less common, mesenteric vasospasm can also follow elective revascularization procedures for chronic SMA occlusion, in which case vasoconstriction of small- and medium-size vessels is precipitated by early enteral feeding.²⁴ The older mean age of the population has produced a group of people with severe medical problems at risk for this type of mesenteric ischemia. The diagnosis is made at the time of angiography. Radiographic criteria suggesting the diagnosis include (1) narrowing of the origins of multiple branches of the SMA; (2) alternate dilatation and narrowing of the intestinal branches (the “string-of-sausages” sign); (3) spasm of the mesenteric arcades; and (4) impaired filling of the intramural vessels.²⁵ The mortality of this specific subset of patients is relatively high regardless of treatment, owing to the serious underlying medical conditions and the frequent delay in diagnosis.²⁶

Mesenteric Venous Thrombosis

Mesenteric venous thrombosis (MVT) is thrombosis of the veins draining the intestine (inferior mesenteric, superior mesenteric, splenic, and portal veins). The obstruction in venous return leads to edema, distension, and eventual infarction of affected segments. Primary MVT is idiopathic, although given the improved understanding of predisposing conditions, the number of patients in this category is diminishing. Patients in whom a causative factor is identified are said to have secondary MVT. These factors include myriad clinical syndromes, including trauma, surgery, cancer, cirrhosis, pancreatitis, dehydration, and increasingly recognized hypercoagulable syndromes such as polycythemia vera, thrombocytosis, protein C and S deficiency, antithrombin III deficiency, antiphospholipid antibody syndrome, and factor V Leiden mutation (activated protein C resistance).²⁷

Patients with MVT have a somewhat different presentation from those who have ischemia caused by arterial obstruction; the onset of symptoms may be insidious and the findings more subtle. Pain out of proportion to the physical examination is still an essential feature. The test of choice to confirm the diagnosis is contrast-enhanced computed tomography (CT), although duplex scanning and magnetic resonance imaging (MRI) are gaining popularity. Thrombus is located in the superior mesenteric vein in 70% of patients, with portal and inferior mesenteric vein thrombus found in about 30%.²⁸

Symptomatic acute MVT is a lethal disease, with a 30-day mortality of about 25% and a 3-year survival of 35%.²⁸ Patients with evidence of chronic thrombosis fare somewhat better, because collateral venous channels form to augment intestinal venous drainage.

Clinical Presentation and Diagnosis

AMI can appear precipitously with decompensation over hours or insidiously with progression over days. Classic symptoms of AMI include sudden abdominal pain out of proportion to the physical examination, with gut emptying at the onset of pain. The subacute pattern of mesenteric ischemia is characterized by a more gradual development of vague abdominal signs and symptoms. These include less intense and nonspecific abdominal pains with nausea, vomiting, and changes in bowel habits. The abdomen may become distended but still have active bowel sounds.

Predictably, physical signs intensify as the syndrome progresses. In the early phases, signs of peritoneal irritation such as abdominal guarding and rebound are absent. As the bowel becomes more ischemic, necrosis progresses from the mucosal layers to the seromuscular layers. After full-thickness bowel infarction, the abdomen is often grossly distended, with absent bowel sounds and exquisite tenderness to palpation. Bowel infarction can impart a feculent odor to the breath.

Ancillary laboratory evaluations often reveal an increase in hemoglobin and hematocrit, consistent with hemoconcentration. There is a marked leukocytosis with a predominance of immature white blood cells (left shift). Although no specific laboratory findings are diagnostic, serum levels of amylase, lactic dehydrogenase, creatine phosphokinase, and alkaline phosphatase, singly or severally, are often elevated, along with a metabolic acidosis with a persistent base deficit.²⁹ Unfortunately, most of these abnormalities do not develop until after bowel necrosis has occurred.

Plain abdominal radiographs are used to exclude other potential causes of abdominal pain rather than confirm the diagnosis of AMI. In fact, completely normal plain abdominal films are seen in more than 25% of patients with mesenteric ischemia.³⁰ Subtle signs of AMI on plain abdominal films include a dynamic ileus and distended air-filled loops of bowel. Bowel wall thickening from submucosal edema or hemorrhage can be prominent, especially in cases of acute MVT. In advanced stages, pneumatosis of the bowel wall and portal vein gas portend an extremely poor prognosis.

Barium contrast evaluations of the upper and lower gastrointestinal tracts are contraindicated because residual intraluminal contrast material can limit visualization of the mesenteric vasculature during diagnostic angiography. On the rare occasion when barium studies are performed in a patient with the gradual development of abdominal pain, the submucosal edema and hemorrhage of intestinal ischemia are manifest by thickening of the bowel wall, strictures, or ulcerations.

Duplex ultrasonography may be of some benefit in visualizing flow in the SMA and celiac axis. With expert technical assistance, these tests can document proximal stenoses in the SMA or celiac axis or complete occlusion of these vessels.³¹ In newer series, color Doppler ultrasonography has been shown to be a valuable screening tool for AMI; it is far more specific than clinical evaluation alone.^32,33 Unfortunately, a significant percentage of patients at risk for mesenteric ischemia have dilated air-filled loops of bowel that make ultrasonography difficult if not impossible.

CT of the abdomen and pelvis can delineate subtle changes consistent with subacute bowel ischemia such as focal or segmental bowel wall thickening.³⁴ Thrombus within the mesenteric veins or the lack of opacification of the veins after intravenous contrast administration is often seen in MVT.³⁵ Nonenhancement of the arterial vasculature with timed intravenous contrast injections can be noted in acute mesenteric arterial thrombosis or embolization. CT scans can also vividly demonstrate pneumatosis or portal vein gas.

Advances in contrast-enhanced and cine phase magnetic resonance angiography have allowed better visualization of the visceral vasculature and have a more important role in the diagnosis of AMI.³⁶ Specifically, when MRI is coupled with magnetic resonance oximetry, both anatomic and physiologic information regarding the mesenteric circulation can be obtained.³⁷

Despite these aforementioned developments, the definitive diagnostic study remains mesenteric angiography via either CT angiography or catheter-based studies if the former is not available. Image manipulation (three-dimensional reconstruction) or multiple views are often needed for adequate assessment of the vessels at risk. The origins of the celiac axis and the SMA can be visualized only by lateral views, whereas the more distal celiac axis and SMA distributions are best viewed through anteroposterior projections. On occasion, selective cannulation of the origins of the celiac axis and SMA is often required to completely define the anatomy and pathophysiology. Thorough aortography is also needed to evaluate potential inflow and outflow sites for bypass grafts, as well as to clarify the extent and location of other atherosclerotic lesions in the iliac artery and the IMA.

In patients with nonocclusive ischemia, angiography usually reveals multiple areas of narrowing and irregularity in major branches. The small- and medium-size arterial branches may be decreased or absent, and the vasculature is diffusely pruned, with an absent submucosal “blush.” In MVT, selective angiograms may demonstrate reflux of contrast material back into the aorta owing to extremely slow flow and heightened outflow resistance. A prolonged arterial phase with accumulation of contrast and thickened bowel walls is also characteristic. In extreme cases, angiographic contrast may extravasate into the bowel lumen, which is indicative of active bleeding. The definitive diagnosis of MVT is made during the venous phase; either a filling defect is noted within the portal vein or, in more severe cases, the entire venous phase is absent.

Treatment Options

Initial treatment of AMI includes volume resuscitation, correction of acidosis, and administration of appropriate antibiotics. Heparin anticoagulation should be started immediately to prevent further propagation of thrombus. A urinary catheter, as well as a peripheral arterial catheter, should be placed for monitoring intravascular volumes and hemodynamic status. A nasogastric tube should be placed to decrease the chance of aspiration.

Contrast-enhanced imaging studies, such as CT angiography, should be performed immediately. Although mesenteric angiography remains a definitive diagnostic tool, it is increasingly used in association with planned endovascular treatment. In select patients with an early diagnosis of SMA embolus unassociated with bowel necrosis, a trial of thrombolytic therapy and angioplasty may be appropriate.^38,39 Such treatments are usually limited to patients with abdominal pain for less than 8 hours’ duration without signs of peritoneal irritation. If lysis is not evident within 4 hours of commencing high-dose thrombolytic therapy, or if peritoneal signs develop, the infusion should be discontinued and immediate surgical exploration should be performed.

An increasing number of case reports and series have detailed the use of percutaneous angioplasty to dilate significant atherosclerotic plaques of the SMA that are unmasked by thrombolytic therapy.^40–42 Owing to the variable angle of the origin of the SMA from the aorta, placement and removal of the angioplasty catheter and stent placement may be more difficult than for lower extremity angioplasties.¹⁰ Restenosis rates range from 25% to 50% in earlier series,^40,41 but the largest single-center retrospective review to date demonstrated more promising results. In a 9-year series of 70 patients with AMI, the Cleveland Clinic vascular group achieved an 87% success rate in endovascular treatment of AMI. Patients in the endovascular group were slightly older (65 ± 12 vs. 60 ± 13 years), were weighted with more thrombotic occlusion cases (72% vs. 64%), and had longer duration of symptoms (median, 62 vs. 26 hours). The primary mode of endovascular treatment was thrombolysis infusion; additional therapy included vasodilator (papaverine or nitroglycerin) therapy (51%), mechanical thrombectomy (12%), and PTA plus stent (33%). Successful endovascular therapy resulted in fewer laparotomies (69% vs. 100% in traditional therapy), lower rates of acute renal failure (27% vs. 50%) and pulmonary failure (27% vs. 64%), and lower mortality rates (36% vs. 50%).⁴³ Those who failed endovascular treatment had the same high 50% mortality rate as the open surgical group. Still, while endovascular therapy is increasingly used for AMI at major center, open surgical revascularization remains the predominant treatment across the United States.⁴⁴

When an aortic dissection involves the origin of one or more of the visceral vessels, endovascular repairs have been attempted through stent placement^45,46 and balloon fenestration of the dissection septum.⁴⁷ Although such minimally invasive treatments are highly attractive, they are currently limited by the frequently rapid onset of ischemic symptoms, inability to gain access to the dissection channel, or the need for surgical repair of an associated aortic aneurysm.

Regardless of the cause, most patients with acute arterial occlusion require early surgical exploration and reestablishment of mesenteric flow to prevent or minimize bowel infarction. A generous midline incision should be made, and the extent of mesenteric ischemia and necrosis should be assessed. If the entire small bowel is frankly gangrenous, enterectomy with lifelong hyperalimentation is the only option. In many instances, patient preferences and family consultation may argue for simple abdominal closure with terminal pain relief as a more appropriate choice. If bowel infarction is not profound, surgical revascularization should be performed.

To achieve adequate exposure, the transverse colon is retracted superiorly, and the fourth portion of the duodenum is mobilized to the ligament of Treitz. The SMA is identified by palpation of the root of the mesentery. If the cause of mesenteric ischemia is an embolus, a more proximal SMA pulse is often noted. The SMA is encircled at or just distal to the level of obstruction (Figure 23-3A), and a transverse arteriotomy is made. Balloon-tipped embolectomy catheters are inserted retrograde, and the embolus is extracted (see Figure 23-3B). Embolectomy catheters should also be passed distally to ensure that no fragmentation of the clot or discontinuous thrombosis has occurred. Transverse arteriotomies are closed primarily with interrupted fine monofilament sutures to ensure that the vessel is not stenosed (see Figure 23-3C). If a longitudinal arteriotomy is required, closure is best accomplished with a vein patch. Appropriately selected longitudinal arteriotomies can also be used for distal anastomoses of bypass grafts if thrombectomies are unsuccessful in obtaining arterial inflow.

FIGURE 23-3 A, Mobilization of the transverse colon and duodenum to expose the superior mesenteric artery. B, Balloon-tipped catheter extraction of a mesenteric embolus through a transverse arteriotomy. C, Primary closure of the arteriotomy without stricture.

(From McKinsey JF, Gewertz BL: Acute mesenteric ischemia. Surg Clin North Am 77:307–318, 1997.)